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Oecologia (1995) 101:329-334
9 Springer-Verlag 1995
S. Arizaga 9E. Ezcurra
Insurance against reproductive failure in a semelparous plant:
bulbil formation in Agavemacroacanthaflowering stalks
Received: l March 1994 / Accepted: 22 September 1994
Abstract Bulbils are small aerial rosettes that occur on
the flowering stalks of semelparous Agave plants and in
related families, and that are capable of acting as clones
of the parent plant. We hypothesized that bulbil formation was inversely related to fruiting success in the flowering stalk, and we explored this hypothesis in A. macroacantha, a species from South-Central Mexico. Forty
randomly chosen plants were divided amongst three
treatments: (a) elimination of all floral buds, (b) exclusion of pollinators, and (c) control. We also studied 22
plants in which the flowering stalk had been felled by
goat grazing. Between September and November 1991
we kept a record of the numbers of bulbils and capsules
produced in each flowering stalk. Significant (P<0.0001)
differences between treatments were found in the proportion of plants bearing capsules and bearing bulbils. The
control treatment had the highest proportion of plants
producing capsules, treatment a had the highest proportion of individuals bearing bulbils, while treatment b
showed an intermediate response. In the goat-grazed
group, 45% of the plants failed to produce any propagative structure after the stalk was cut, and half of all plants
produced bulbils on the remaining stump. A significant
inverse relationship between the numbers of capsules
and the numbers of bulbils per plant was found for the
three randomly assigned treatments. Our results suggest
that once the production of the flowering stalk has been
triggered and the death of the rosette is irreversible,
bulbils may act as an insurance mechanism that increases
the probability of successful reproduction of the genet.
Key words Semelparity 9 Vegetative reproduction
Bulbil 9Agave
S. Arizaga(~) 9E. Ezcurra
Centro de Ecologfa,UniversidadNacional Aut6nomade M6xico,
Apartado Postal 70-275,04510 Mexico, D.F.
Introduction
The production of small aerial rosettes (known as bulbils) on the tall flowering stalks of semelparous Agave
plants is frequently observed in North American drylands. The adaptive importance of these structures, if
any, has been unclear. It is well known that agaves can
propagate vegetatively through basal shoots and rhizomes, and it seems self-evident that shoots rooted in the
ground should have a greater chance of survival than unrooted rosettes exposed to the dry desert environment
1-5 m above the ground. In this paper we report data on
the mechanisms that trigger bulbil formation in Agave
macroacantha in southern Mexico, as part of a longerterm study on the reproductive and cloning mechanisms
of Agave spp.
The genus Agave (Agavaceae) consists of succulent
monocotyledonous plants with leaves arranged in basal
rosettes. Agaves are native to the American continent
and show their maximum diversity in Mexico, mostly in
the dry regions. The capacity to accumulate water in the
thick succulent leaves makes the genus especially adapted to aridity (Gentry 1982). These plants can propagate
by two mechanisms: (a) the production of seeds through
sexual reproduction of the semelparous rosettes, and (b)
vegetative multiplication, or cloning; cloning is achieved
in three different ways, by forming (i) bulbils, (ii) basal
shoots, or (iii) rhizomatous suckers (Gentry 1982, 1985).
Bulbils are small aerial shoots forming little rosettes on
the meristems of the inflorescence (Gentry 1982; Robert
and Garcfa 1985; Lock 1985; Nobel 1988). These rosettes are frequently shed through abscission as the stalk
dries out, or fall to the ground with the dead stalk if it is
mechanically damaged (Fig. 1). Basal shoots are ramifications from the lower axillary meristems of the rosette,
forming new rosettes that emerge on the periphery of the
parent plant and produce adventitious roots which allow
their independent growth (Gdmez-Pompa 1963; Gentry
1982; Lock 1985). Finally, suckers are shoots produced
from rhizomes (i.e., subterranean stems generated from
the base of the rosette) and emerge at a distance from the
330
Fig. 1 Bulbils of Agave macroacantha at the top of a flowering stalk, around 3 m above the
ground. A capsule is also seen
in the lower right corner of the
plate. The vertical scale is
10 cm
parent plant (Nobel 1977, 1988; Gentry 1982; Barrientos
et al. 1985).
Bulbils are sometimes planted to propagate cultivated
species like A. fourcroydes (Gentry 1982), A. tequilana
(Robert and Garc~a 1985) and A. sisalana (Bm-rientos et
al. 1985; Lock 1985; Nobel 1988). The procedure allows
clonal increase of a given genetic stock, although it also
facilitates the propagation of viral diseases (Barrientos et
al. 1985). BulbiI formation is not exclusive to the Agavaceae, but is present in other families, especially in other monocotyledons that are taxonomically related to the
Agavaceae (Table 1). Because bulbils occur in flowering
structures, they have been often confused with viviparous seedlings (G6mez-Pompa 1963; Bell 1991). In the
context of this frequent confusion, Bell (1991) defined
bulbil formation as "false vivipary".
In many Agave species plants with the inflorescences
covered with bulbils and with very few or no capsules
with seed are frequently observed in the field (Table 1).
On the other hand, plants that produce a high number of
capsules usually have few or no bulbils. This pattern suggested to us that bulbil formation is, in some way, inversely related to fruiting success. This hypothesis has
also been put forward by Hodgson et al. (1989) for Agave murpheyi in Arizona. These authors noted that when
freezing temperatures occur during flowering, "flowers
are produced but abort, and are replaced by vegetative
bulbils". Their published observations, however, are not
supported by quantitative data. We explored this hypothesis in A. macroacantha Zucc., an endemic species from
the Valley of Tehuacfin-Cuicatla6 in south-central Mexico (Gentry 1982) that produces both capsules and bulbils
in the flowering stalk, and also propagates by means of
basal shoots and suckers.
Trade-offs between sexual reproduction and asexual
propagation have been described in detail by many au-
thors (e.g., Sarukhfin 1976; Willson and Price 1977;
Wid6n t992; for reviews see Abrahamson 1980; Fenner
1985; Bazzaz and Ackerly 1992; Stearns 1992). At a developmental level, van der Pijl (1972), Faegri and van
der Pijl (1971), Solbrig (1976), and Wid6n and Wid6n
(1990) have documented in detail the relationship between the process of fertilization and the formation of
vegetative structures. In Agave the normal vegetative
structures that propagate the individual ramet are the
basal shoots and suckers. In this paper, however, we analyze a different phenomenon, occurring at a smaller scale
than the whole ramet. Our study evaluates the relationship between flower and bulbil production, not within
the whole plant, but specifically at the level of the flowering stalk and after the stored nutrients have been mobilized to the flowering (i.e., normally sexual) reproductive
structures.
Methods
Our field observations were made between April and November
1991, at the Helia Bravo Botanical Gardens, 30 km south of the
city of Tehuacfin, Puebla. Mean precipitation is 400 mm (Garcfa
1981) and the prevailing vegetation type is a dry xerophytic scrub
(Rzedowsky 1978) dominated by Neobuxbaumia tetetzo, a giant
columnar cactus (Zavala-Hurtado 1982). The monsoon-type rainy
season in this region starts in late May, and ends in late September.
A. macroacantha produces flowering stalks in April and May. By
September-November the capsules are ripe and start to open.
In April and May 1991, we randomly chose 50 plants from an
area of approximately 2 ha, and divided them randomly amongst
three treatment groups: (a) elimination of all floral buds from the
inflorescence by clipping (n=12), (b) exclusion of pollinators with
a gauze net (n=12; this treatment did not exclude the possibility of
fertilization by airborne pollen), and (c) control (n=26). We also
marked 12 plants in which the flowering stalk had been felled by
goat grazing, randomly selected from a set of goat-grazed individuals (goats frequently nibble the stalks until they fall, and then eat
331
Table 1 Bulbiferous species from different plant families, taken
from the literature
Family
Species
Monocotyledons
Agavaceae
Agave aktites
A.
A.
A.
A.
angustifolia
breedlovei
cantala
cantala
var. acuispina
A. chrysantha
A. decipiens
A. fourcroydes
A. guiengola
A. macroacantha
A. murpheyi
A. neglecta
A. parvidentata
A. parviflora
A. polyacantha
A. sisalana
A. toumeyana
A. weberi
A. werchlei
A. arizonica
Araceae
Cyperaceae
Dioscoreaceae
Gramineae
Iridaceae
Liliaceae
Musaceae
Orchidaceae
Zingiberaceae
Gentry1982
Gen~y1982
Gentry1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Gentry 1982
Powers &
Blackhaus 1989
A. karwinski
G6mez-Pompa 1963
Cave 1964
Furcraea andina
Alvarez 1986
Furcraea gigantea
Furcraea hexapetala
Alvarez 1986
Alvarez 1986
Furcraea macrophylla
Mabberley 1987
AmorphophaIlus bulbifer
Mabberley 1987
Remusatia viviparum
Bell 1991
Cyperus alternifolius
Passam et al. 1982
Dioscorea alata
Passam et al. 1982
D. bulbifera
Dactylis glomerata
Bell 1991
Bell 1991
Deschampsia alpina
Festuca ovina vat. vivipara Bell 1991
Homeria breyniana
Mabberley 1987
Allium oschaninii
Mabberley 1987
Allium cepa var. viviparum Bell 1991
Bibiloni et al. 1987
Brimeura fastigiata
Bell 1991
LiIium bulbiferum
Hanks 1987
Narcisus spp.
personal observation
Heliconia spp.
Mabberley 1987
Cynorkis uncata
Bell 1991
Costus spiral&
Globba propinqua
Bell 1991
Dicotyledons
Brassicaceae
Dentaria bulbifera
Polygonaceae Polygonum viviparum
Ranunculaceae Ranunculusficaria
Saxifragaceae
Reference
subsp.bulbifer
Saxifraga cernua
S. granulata
Mabberley 1987
Mabberley 1987
Mabberley 1987
to test the significance of differences between treatments (McCullagh and Nelder 1983). In these models, the measure of deviance
(i.e., the squared differences between the observed values and the
values expected under the null hypothesis) is the G statistic (Sokal
and Rohlf 1981), which is distributed as ;(2, and is the appropriate
measure of dispersion for frequency data. To avoid the error introduced by low expected values, we lumped categories in which
these values were too low by adding them to contiguous classes
(Sokal and Rohlf 1981).
The relationship between production of seeds and production
of bulbils was evaluated by a principal-axes analysis (Sokal and
Rohlf 1981), as both variables were equally subject to random error and it was not possible to define which should be considered
the dependent variable. The goat-grazed group was not included in
this analysis for two reasons: (a) it was not a random treatment,
and (b) an ANOVA of the residuals of the principal axis line (calculated as the second component axis) for all four groups together
showed that the goat-grazed group differed very significantly from
the rest (P<0.0001), while the three random treatments did not differ significantly in the distribution of their residuals. Additionally,
the inclusion of the goat-damaged group caused the residuals to
fail the standard tests for constant variance (homocedasticity), and
for lack of outliers and serial correlation (Draper and Smith 1981).
Thus, the principal axis line was calculated only for the three randomly assigned treatments.
To analyze the possible effect of other unknown factors on the
number of structures per plant, the variation within treatments was
tested for randomness by calculating the probability of their residual X2 [Z(observed frequency - treatment mean)Z/treatment mean]
under the null hypothesis that the within-treatment variation was
random. For simpler interpretation, the residual Z 2 was divided by
the degrees of freedom of the treatment (n-l), to calculate the
variance-to-mean ratio (V/m), an indicator of randomness. V/m approaches unity in random Poisson frequencies, and is higher than
unity in clumped, non-random distributions (Greig-Smith 1983).
Results
Significant (P<0.0001) differences between treatments
were found in the proportion of plants bearing capsules,
the proportion bearing bulbils and the proportion bearing
no propagation structures (Fig. 2; the proportions do not
necessarily add up to 100%, as some plants may produce
both capsules and bulbils). The control treatment had the
highest proportion of plants producing capsules and the
lowest proportion of plants producing bulbils. Treatment
100
8o
or
60
Mabberley 1987
Mabberley 1987
40
2o
n-
the flowers). Although we also analyzed the results from this last
group, for comparative purposes, it cannot be strictly considered a
random sample o f the flowering plants, as goat grazing may be
non-random. During the experiment, goat grazing reduced our
sample size in treatment b to 9 individuals, and in the control
group to 19. Accordingly, the goat-grazed group increased to 22
plants. Between September and November 1991, we kept a record
of the number of bulbils and the number of capsules with seed that
were produced by each flowering stalk.
As our dependent variables were frequencies in all cases (i.e.,
counts of plants, capsules, or bulbils), log-linear models were used
o
Control
Excluded
Pruned
Consumed
Treatment
Fig. 2 Relative frequency of rosettes bearing capsules (solid
bars), bulbils (vertically striped bars), and bearing no propagative
structures (diagonally shaded bars) in their flowering stalks for
the different treatments. The absolute frequencies are given in parentheses at the top of each bar. The proportion of plants bearing
capsules, bulbils, and no structures varied significantly among
treatments (Z2=28.6, df=6, P<0.0001)
332
14
25
21
'2i
17
.13
15
lO
:5
=
'~
.13
0
10
8
4
9
i
6
d~
E
"1
Z
q
E
X
X
r
5~
0
i1~ ~
0
9
9
~
...............................................
5
10
o
.........
0
15 17 21 25
o
2
Number of c a p s u l e s
Fig. 3 Numbers of capsules plotted against numbers of bulbils in
flowering stalks from the different treatments [circles control
plants (n=19), triangles pollinator-excluded plants (n=9), squares
plants where floral buds were pruned (n=12), crosses goat-felled
plants (n=22)]. The treatments differed significantly both in the
number of capsules (Z2=34.8, df=-6, P<0.0001), and of bulbils
(X2=14.0, df=6, P=0.03)
a (elimination of flower buds) had the lowest proportion
of individuals bearing capsules and the highest with bulbils, while treatment b (pollinator exclusion) showed an
intermediate response. In the goat-felled plants, a large
proportion (45%) failed to produce any propagation
structure after the stalk was cut, a few individuals regenerated new branches and some capsules on the old
stump, and half of all plants produced bulbils on the
bracteal meristems of the remaining flowering stalk.
The same trend as that described in the previous paragraph for whole plants was observed for the number of
structures per plant. On average, the highest number of
capsules and the lowest number of bulbils were found in
the control plants. Treatment a (elimination of flower
buds) had the lowest numbers of capsules and the highest
numbers of bulbils, and treatment b (pollinator exclusion) showed an intermediate response. Our current investigations of the reproductive system of A. macroacantha suggest that this species is strongly self-incompatible. The capsules formed in the pollinator-excluded
treatment are probably the result of wind-pollination.
These three treatments defined a significant (P<0.0001)
principal axis line showing that these structures have
some functional equivalence and can replace each other
(Figs. 3 and 4). The analysis of the residuals showed that
the goat-felled plants lie significantly below this line.
Their joint production of capsules and bulbils was lower
than in any other treatment, as the felling of the stalk
eliminates a substantial amount of biomass and active
meristems. With only one exception, the frequencies
within all treatments were not randomly (Poisson) distributed around the treatment mean (Table 2). This indi-
4
6
8
10
12
14
M e a n number of c a p s u l e s
Fig. 4 Principal axis analysis of number of capsules against number of bulbils. Symbols as in Fig. 3. A significant negative correlation was found between the number of bulbils and the number of
capsules for the three randomly assigned treatments (r= ~0.31,
n=40, P=0.05; in each treatment taken separately the two variables
were uncorrelated). The slope of the axis line (bulbils=12.2 -1.3
capsules) was significantly different from zero (P<0.05). For clarity, only the mean of each treatment, and the ellipse corresponding
to the bivariate standard error of that treatment, are given
Table 2 Variance-to-mean ratio (V/m) in the four treatments for
both numbers of capsules and numbers of bulbils, and significance
(P) under the null hypothesis of randomness of the within-treatment variation. With the exception of the numbers of capsules produced in plants which had the original flowers pruned, the withintreatment frequencies of all other treatments departed significantly
from randomness
Treatment
Control
?/
19
Pollinator
excluded
9
Flowers
pruned
Goatgrazed
12
22
Capsules
V/m
P
9.67
<0.0001
5.00
<0.0001
6.41
<0.0001
14.86
<0.0001
1.51
0.12
2.43
<0.0003
Bulbils
V/m
P
9.37
16.37
< 0 . 0 0 0 1 <0.0001
cates that although the treatments accounted for a significant part of the observed variation, within treatments
some individual plants produced a significantly higher
number of structures than others, possibly as a result of
other ecological factors not considered in our design.
Discussion
One of the main demographic risks in the life history of
long-lived semelparous plants is the threat of total reproductive failure induced by random environmental events.
333
However, it can be seen that most long-lived plants usu- bivores (insects and rodents) often consume flower parts
ally cited as semelparous can, and often do, multiply (Eguiarte y Bfirquez 1987), while large herbivores can
vegetatively by suckers and basal shoots. Thus, the indi- consume or break the whole flowering stalk. Introduced
vidual ramet may be semelparous, but the whole genet is large grazers which did not evolve in interaction with the
often iteroparous. In this way, cloning may act as a way local flora often have an even greater effect than the native herbivores (Crawley 1983; Hart and Norton 1988;
of bet-hedging against long-term reproductive failure.
At the level of the individual ramet, however, semel- Tucker and Leininger 1990). This is clearly the case with
parity poses a special challenge to long-lived plants. In goats in our study zone, which destroy whole flowering
Agave, for example, the mobilization of metabolic re- stalks and have been reported to be one of the main causserves stored in the base of the rosette seems to be an ir- es of environmental degradation in the region (Smith
reversible physiological process. Once the development 1965; Meyrfin 1980). Nectarivorous bats of the genus
of the flowering shoot has been triggered and the basal Leptonycteris (Glossophaginae), the main pollinators of
reserves begin to be hydrolyzed and translocated, the fi- Agave spp., are migratory and may fail to arrive in synnal reproductive effort and the ensuing senescence of the chrony with the brief mast-flowering period of the flowrosette cannot be reversed (Howell and Roth 1981), al- ering stalks (Howell 1979; Howell and Roth 1981; Arita
though in some cases severe damage to the inflorescence and Humphrey 1988; Arita 1991). In any of the above
may prolong the life of the plant for some time (Nobel cases, the result is the death of the rosette producing lit1988). This fact is the basis for the production ofpulque tle or no viable seed. Our results suggest that once the
(a fermented brew obtained from Agave sap), and is well production of the flowering stalk of A. macroacantha has
known by Mexican peasants. If the apical meristem and been triggered and the subsequent death of the basal rothe central core of the stem are carved out before flower- sette is irreversible, the production of bulbils may act as
ing starts, the plant will continue mobilizing sugar-rich an insurance mechanism that recovers metabolic resourcsap from the leaves into the hollow cavity thus formed in es that have been mobilized, and increases the probabilithe center of the rosette until the plant dies (Gentry ty of successful reproduction of the genet. We do not
1982; MNCP 1988). Pulque farmers can predict when a know how generalized this response is in other Agave
plant is going to flower by the thinning of the central species, but our field observations on other agaves sugleaves of the rosette and by a change in the color and as- gest that the phenomenon may be common.
pect of the lateral leaves during the previous growing
season (MNCP 1988). This suggests that the floral struc- Acknowledgements We want to acknowledge the enthusiastic
of Ernesto Vega during the field work, and the helpful comtures in Agave are preformed at least a year before flow- help
ments from two anonymous reviewers and from Maureen Stanton.
ering occurs.
This paper is part of the first author's postgraduate research at
Quite obviously, if successful reproduction fails (e.g., UNAM.
through unsuitable environmental conditions, lack of
pollinators, or excessive flower predation), though the
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